SPIDER SEX

(This article is part of a series on spider behavior- if you haven’t read my Introduction to Spiders yet, find it here!)

Yup, it’s happening. We are going to learn all about the twisted, terrifying, and occasionally quite kinky world of spider sex.

You would think that I could not fill up a whole article on the topic of spider sex- after all, sex is sex, right? Tab A into slot B, and bam, done: that’s sex. Not for spiders, though. Not only have they added a whole extra step to the basic mechanics to the act, but even getting a chance to mate can be an extreme challenge. I’m sure right about now you’re all considering the use of “widow” in the name black widow, but sexual cannibalism is actually only a small part of the spider sex story.

Yeah. The spider sex story.

THE SPIDER SEX STORY

It all begins when the male spider ejaculates.

Does that seem a little late for a starting point? Actually, for spiders, the act of ejaculation long precedes the actual act of fertilization. No female is even close to the male when this occurs, and he probably won’t meet one for a long while.

You see, male spiders have no penises with which to transfer sperm to females. In place of any abdominal genitalia, they have a simple hole called the gonophore on the underside of their abdomen. When the spider ejaculates, sperm simply falls out of this hole. This would make mating rather difficult, because as I mentioned before, the male spider ejaculates before a female is even present- actually, he ejaculates pretty much as soon as he is physically capable of doing so. (I’m sure some of my readers can relate.)

To prevent the sperm from just falling on the ground, the male spider spins a little web underneath his abdomen, kind of like a spider-diaper, to catch the sperm when it falls. He then contorts himself so that he can suck up the sperm into needle-like appendages within his pedipalps. This is often referred to as “charging” the palps.

Is this making you uncomfortable? I’ll try to go into a bit more detail.

I discussed spider pedipalps in the previous article: they’re two appendages on either side of the spider’s mouth that look like small legs. On males, the tips are usually enlarged… for reasons.

A handsome striped lynx spider showing off his enlarged pedipalps.

If you flip the spider over, it quickly becomes apparent that those fuzzy things aren’t just used for dusting. Underneath the palp lies a coiled organ called a palpal bulb, containing a sperm duct and ending in a needle-like point called an embolus. This organ works like a turkey baster. It can suck sperm up… and when needed, it will spit it out again.

A close-up of the pedipalp of a goblin spider. This is an example of a simple male pedipalp; others can get ridiculously complex, with tubes and frills everywhere. (From Izquierdo & Rubio, 2011.)

So, when the male spider does finally meet a female and get with the doin’, it is these pedipalps he inserts into the female spider’s paired spermatheca (i.e., sperm storage organs). We’ll get to the female half of things in a moment, but first, let’s talk about those pedipalps. Because it’s weird, right? Why transfer sperm in such a complicated way when so many other creatures manage to make the process so easy?

The story- the theorized story, anyway- is perhaps more interesting than you might think. First, we have to remember that while intravaginal sex seems pretty normal to us, it evolved long, long after our lineage split with the arthropods, the group that includes insects and arachnids. In fact, the arthropods that do practice a form of sex that we’d consider more “traditional” (abdominal genital inside other abdominal genital) actually evolved the practice entirely separately from us.

What happened before internal fertilization, then? Well, we still see it today in many of our aquatic cousins, the fish: the male simply sprays his sperm over the female’s eggs. Easy-peasy. The earliest arthropods, which were also aquatic, did the same thing.

But when arthropods and vertebrates both started to leave the water, a change had to occur. Sperm evolved to swim through liquid to get to eggs, so if a male ejaculated on dry land, the sperm would obviously not make it. Similarly, eggs released without some kind of waterproof covering- like an eggshell- would just dry out. This is why amphibians must fertilize their eggs in the water.

Contrary to what you might think, there is nothing internal going on here. (Photo source.)

But for other animals, some major mechanical changes had to take place.

Most land vertebrates engineered the “butt bump” style of mating: they got one hole to connect to the other, somehow, so that the sperm wouldn’t dry out and could get to the egg before it took on its protective covering. And some arthropods stumbled upon this strategy as well. However, as far as arachnids (as well as many insects) go, there was an even better solution: sperm packaging, in the form of spermatophores.

I won’t delve too deeply into spermatophores, since we have a lot of other things to cover today. However, most spiders do not use spermatophores, which are literal packages of sperm that a male gives to a female. Instead, it’s assumed that this was probably an ancestral trait of theirs, since almost all other arachnids do use them. From spermatophores, presumably, rose the spider habit of gently maneuvering the sperm packages into the female with one’s pedipalps, until eventually male pedipalps evolved into a specialized organ for this exact purpose. To put it another way, spiders converged on an extremely roundabout route to sex that looks similar to ours… if male humans had their penises on their faces.

There are both drawbacks and advantages to transferring sperm in this way. The drawback is that it takes a male spider a lot of time and energy to get ready for copulation, more than it would for, say, a male mammal. However, in some species, the male spider makes up for this by ensuring his paternity. He may, after inserting his sperm, deposit a special plug to prevent the female from mating with anyone else. Or, in more extreme cases, the male spider may actually break off his pedipalps, in an act the literature unfacetiously calls “genital mutilation,” in order to keep them lodged eternally within the female.

Just super great stuff.

But we’ve been focusing on the males way too much. It’s not as if the females just passively sit around and wait to be fertilized, after all. The process of laying eggs is far too costly (sometimes it costs her life!) to just take in any old sperm. It had better be the best sperm available, or consequences may be dire.

As I mentioned before, female spiders have paired spermatheca organs for the male to insert his pedipalps into. These organs can just hang onto sperm until the female ovulates, in which case the sperm kind of gets shot through a loop so that it passes over and fertilizes the descending eggs before the spider lays them. In most female spiders, there are actually three reproductive tracts: two for the male to insert his pedipalps into, and one in the center where the eggs come out.

Sadly I could not find a good (fair use) photo of female spider genitalia. I know you all are extremely disappointed.

Here is Spiderman’s abdomen instead.

The advantages to storing sperm like this means that female spiders can actually pick and choose which sperm get to fertilize their eggs by only allowing males to inseminate one out of two spermatheca- thus enabling them to remember whose sperm went where. They can also choose to eject the sperm entirely if necessary. So if they hang on to the sperm of a questionable male and nobody better comes by, well, better to have crappy genes than none at all. Otherwise, if Mr. Spider Right comes by, that old sperm gets tossed out like used cat litter.

The length of the tubes connecting the spermatheca to the oviduct is variable between different species- some have barely any separation at all, while some are fantastically elongated and looped multiple times. The reason for these differences is possibly due to an evolutionary arms race between male and female genitalia: the emboli of male palps grow longer in order to bypass female mate choice by directly depositing the sperm in the oviduct, whereas the female spermatheca grow longer to prevent this. I am not kidding about the looped and longer parts- in some diagrams, female copulatory ducts look like a child’s scribbles with all their twists and turns.

Like this one, comparing the reproductive tracts of two different species. The two circles are the spermatheca, the squiggly bits are the ducts leading into them. (From Eberhard & Huber, 2010.)

You can see why some male spiders might try to take other, more drastic measures to give their genes a fighting chance.

What about these measures, then? Thus far, we’ve mostly talked about the mechanics of spider sex in general terms. Sperm meets egg, etc. But as with many animals, there is more to the story than that: not only do spiders have to make things mechanically complicated, they have to make things behaviorally complicated, too.

Let’s delve into the questionably kinky world of spider mating rituals.

SPIDER FLIRTATION PART ONE: THE PEACOCKS

The gif I posted up at the very top of this article is of a peacock spider (Maratus sp.), and it is part of a spider group rapidly becoming familiar to the internet consciousness. It’s not hard to see why: as a subset of jumping spiders, peacock spiders are mandatorily adorable, and the flashy displays of the males just push this genus over the edge.

Here is footage of one species of peacock spider (Maratus speciosus) performing his courtship dance.

See? Doesn’t that make up for all those horrifying descriptions of spider genitals from earlier? …No?

Ok, well, anyhow, as you may have guessed, the male spider uses his colorful “fan” in the same way that the spider’s namesake, the peacock, uses his. (The spider’s fan is actually an upraised abdomen with outstretched abdominal flaps, but we won’t quibble here.) It is used as a means to get the female’s attention and probably proves something about that particular male’s genetic quality.

As to what that might be… nobody really knows. The study of this particular group is relatively new to science, as new species are still being discovered, each with its own particular display patterns and dance moves.

To help explain how something so flashy could go unnoticed for so long, I am providing this helpful size comparison. (Photo by Jurgen Otto.)

By the way, the visual display is only a part of what the male spider is trying to impress with- the other part we just aren’t sensitive enough to feel. But female peacock spiders, bless their single-chambered hearts, are just sensitive enough. During courtship, the male peacock spider stridulates his abdomen, sending out specialized little vibrations for the female to pick up with her legs. He also drums with his forelegs, occasionally on the female’s head. Do you understand yet how sexy he is, lady?

Like the visual displays, these acoustic displays vary by species, and by situation. In fact, the spiders seem to mix and match visual and acoustic displays depending on the environment they meet the female in. If she’s far away and out of sight, acoustic displays will get her attention; if she’s close up, add the visual component to the mix.

Even without adding variations based on the environment, you might have noticed in the video above that the dance of the peacock spider can be quite long and complex. Not only does the male display and vibrate his abdomen, he also raises his third pair of legs (which are also modified with species-specific fringes and colors) and waves them in all different directions. Many species add in even more moves, like flapping their abdominal flaps and pedipalp waving (equivalent to a male human whirling his junk around). About the only thing all the dances of all the different species of peacock spider seem to have in common, in fact, is the very end of the dance: the male will stretch his first and third pairs of legs over the body of the female. If he’s lucky, she’ll allow him to mate with her after that.

Peacock spider dance moves shown in what may be my favorite scientific figure of all time.(From Wearing et al, 2014.)

It really does beg the question as to why these dances need to be so complex, and again, the answer is that nobody yet has a clue. Certainly there might be some evolutionary pressure to differentiate one species’ moves from another, but that can’t explain everything- many spiders already have evolved a good, non-flashy system for this in their pedipalps and spermatheca: the pedipalps of one species generally only fit into the spermatheca of the same kind, like a lock and key.

Perhaps some of the answer might lie in a crucial difference between the behavior of an animal like a peacock compared to its spider namesake: when a peahen doesn’t like how a peacock is dancing, she doesn’t usually turn around and eat him.

But female peacock spiders will, if they aren’t fond of the male’s display- or even if he’s not even displaying. Like most spider species, they aren’t above a little cannibalism now and then. It’s hard for evolution to maintain perfect hair-trigger attack behaviors if you’re supposed to slow down and try to have sex with potential prey once and a while. Perhaps this is what helped speed the evolution of the extraordinarily flashy and increasingly desperate displays of male peacock spiders: they can’t even get close to a female otherwise!

Interestingly, a number of other insects have taken advantage of this with other species of jumping spiders- there are a handful of flies and moths that mimic spider courtship and territorial behavior in an effort to trick their predators into not eating them. If there are peacock spider mimics like these out there, that would certainly prompt the evolution of harder-to-mimic displays on the part of the real males.

It is certainly a topic that deserves more study. However, we can’t just talk about peacock spider courtship when we discuss spider sex, as interesting as it is. This form of courtship- with flashy, exaggerated visual displays- is actually fairly rare among spiders. Jumping spiders and other spiders that hunt actively have very good eyesight, as I discussed in the previous article. However, most spiders that spin webs do not, and rely much more heavily on detecting vibrations and chemoreception. For males of these species, other tactics are necessary if they hope to have a chance at giving the female their sperm.

SPIDER FLIRTATION PART TWO: THE TEENY SNEAKY SEXERS

Female peacock spiders are noticeably larger than males, which emphasizes some of the danger males are put into during courtship, but in terms of spiders the size difference is trivial. If you want to see a real size difference, you should observe the male and female orb weaver spiders.

A mama spider and her baby? I hope not, because these two spiders are engaged in the act of mating. (Photo source.)

Golden orb weaver spiders show the most extreme version of sexual dimorphism, with the female spider being roughly 1000 times heavier than the tiny male. In fact, in many species of web-spinning spiders, males and females were at first assumed to be separate species; in others, the males have not yet even been discovered!

Size differences are most pronounced in spiders that have a sessile lifestyle, including those that hunt from webs and others like the well-camouflaged crab spiders. Why the difference, though? Initially it was assumed that it was due to the danger of being eaten by the female- could smaller males sneak a mating in undetected? But this seems not to be the case, as it is actually the larger males that have more mating success. Further compounding this theory is the fact that based on phylogenetic data, in most species with pronounced size dimorphism it is the females who have gotten bigger, not the males that have gotten smaller- selection was acting on her, not him. But why?

A giant female orb weaver hangs out with her posse of tiny males. (Photo source.)

The difference may not have to do much with sex, but rather with the lifestyles of these spiders. If the size difference evolved along with the web-spinning lifestyle, females- which are generally the ones that spin the webs- could afford to get bigger, while males- which lead a migratory lifestyle to seek out the sessile females- needed to stay small.

Paradoxically, though, there are some species in which the males did get smaller, notably the males of the tangle-web spiders (Tidarren sp.). Actually, these males get so much smaller that they have to tear off one of their pedipalps before they fully mature because it would be impossible for the spider to function with both. The remaining pedipalp also gets ripped off during copulation- almost immediately- but luckily can continue transferring sperm by itself into the female for roughly four hours.

You use what you got.

Even in spiders with female gigantism rather than male dwarfism, the males’ genitals have to get bigger, because obviously they have to be able to penetrate the female enough to deposit sperm. This has led to a few species of spiders with emboli (the organs at the tips of their palps) that inflate to three or four times the length of their own bodies. Impressive!

I don’t know what to caption this with.

These itty-bitty males have to achieve a monumental task: they have to get close enough to the female spider to mate with her without being eaten on the spot. This is difficult when the females in question are nearly blind: no peacock spider-style ornamentation will help here.

Most males declare their intentions up front via vibrations, love taps, and chemical signals. They pluck the strands of the female’s webs for dances that can go on for literal hours. They have to- if the dance isn’t long enough and the female isn’t impressed, well… you only get to put in one application.

Some spiders in the genus Pisaura move beyond mere strutting and actually offer their potential mates valuable gifts in the form of pre-killed prey items. When offered these gifts, the females grab and eat them, giving the males a chance to swoop in and do the deed.

To be fair, some species- like this giant wood spider- use the wait-until-she’s-eating strategy as their main tactic without providing the food themselves. (Photo source)

However, this gift-giving behavior isn’t always as generous as it first appears. While some males are honest, others use a sneaky ploy: gift-wrapping. By wrapping up their present in silk, they make sure the female takes longer to eagerly unwrap it- giving them more time to copulate while she’s distracted. Some males take this ploy to be outright jerks: they wrap up small inedible items, like seeds or dried insect shells, to give to the female. Needless to say, they have to copulate fast to use this strategy and be prepared to run when the female discovers the deception.

Not many Pisaura males go so far to trick the females this way, though- the risks usually run a little too high. (Though some are actually bold enough to try to snatch the meal back after they’re finished mating!) However, for other male spiders, no risk is too high to ensure their seed is sown. In fact, what would seem a drawback for other males can actually work in their favor.

Sexual cannibalism is usually considered an accident, or just a side effect of having to mate with something like a mantis or spider: if the male gets away, great; if he doesn’t, well… them’s the breaks. But some male spiders have evolved to use sexual cannibalism as an actual asset to their breeding. Not only do they not resist it, some males, like redback spiders, will actually flip their abdomens onto the female’s fangs during mating to encourage her to get eating.

It might seem a little counterproductive to the survival of the fittest to willingly off yourself, but remember, evolution doesn’t necessarily favor the long-lived: it favors the ones that pass on their genes. And surprisingly, letting the females eat them helps the males: as with the gifts from the Pisaura spiders, a distracted female mates for longer, even if what she’s distracted with is eating her partner.

Letting yourself get eaten, of course, means that you won’t be able to mate with any other females, so the males that tend to allow or encourage sexual cannibalism tend to come from those that have very high mortality rates prior to finding their mates. Once they leave their mothers’ webs, their only mission that single instance of sex- they don’t even eat. Most of these males also have fragile pedipalps that break after a single mating episode, so there isn’t much point in them trying to find other mates anyway!

Once the female spider has finished eating her first mate she’s less likely to accept another- she’s full now. So there’s yet another advantage for the redback spider male, who watches serenely from spider heaven: ensured paternity.

(By the way, the more-likely-to-mate-when-she’s-full behavior occurs in most female spiders, not just redbacks. At times, a free lunch may be more valuable than a clutch of eggs, no matter how well he dances.)

Here is a video of a male redback spider performing the death flip:

It may seem like things are pretty rough for male spiders in general (though I’m sure if you were to ask them, they wouldn’t care a whit). However, we need to spare a few thoughts for the difficulty on the ladies’ end. Yes, they may eat the males who don’t please him, but it’s not just out of hunger or genetic snobbery. Having small males hanging out in your web can alert prey items to its presence and make it harder for you to catch dinner. Furthermore, they can even attract predators- and furthermore, they sometimes even steal the female’s food!

And sometimes the male spider is the one who makes sex scary for the female.

For some species, it’s as simple as the male tying up the female with silk to ensure she doesn’t snack on him during mating. Ironically, in the literature, this technique is called a ‘bridal veil.’ Some so-called bridal veils contain a chemical compound that makes the female woozy and docile during mating, while other species concentrate on just tying her up completely.

Maybe a little light spider bondage isn’t too bad; certainly some scientists think that the females might find the chemicals and the experience sexually stimulating. But for some species, the females have it much rougher, and not really in a sexy way. The males of diving bell spiders, i.e., the only fully aquatic spiders, are actually larger than the females. And unlike practically every other spider species, it’s the male diving bell spiders that might cannibalize the females. Researchers only noticed this when they saw females running away from large males- even though larger males are actually the ones they prefer to mate with!

(This preference is possible to observe because even though the males are larger than the females, she still has to twist her abdomen up to allow him to inseminate her. Nonconsensual sex is nearly impossible if you’re a spider.)

The size switch was likely prompted initially by the environment: female spiders, who spin underwater webs to fit inside, can do this more easily while small, while males, who again rove in search of mates, can do this more easily underwater while big. Spider cannibalism is less driven by the sex of the individual than it is by the size. Big eats small.

But while females preferred big male mates, things get dangerous when they get too big. So while males remain larger than females due to the environment and the females’ own preferences, they can’t evolve much bigger- else they’ll never be able to catch a mate.

Don’t feel too bad for all these nervous spiderfolk, though. We’ve learned all about the process of courtship, so now it’s time to delve back in to the deed itself. Because there is more to it to just sticking in a thing and shooting out sperm- and it’s all for the ladies.

IT’S ALL FOR HER: INSENSITIVE MALES MAKE THE BEST LOVERS

Interestingly, and uniquely amongst nearly every other animal, the male sperm transfer organs of spiders (the palpal bulbs) have no nerves and therefore no sensory capabilities. Even insects have innervated phalluses (when they have them at all) but not spiders. As humans we may find this rather disappointing, but there are some other, worse consequences to being numb, as one writer eloquently points out:

Because of the lack of nerves in the palpal bulb, the challenges faced by a male spider attempting to copulate can be likened to those of a person attempting to adjust a complex, delicate mechanism in the dark, using an elongate, elaborately formed fingernail. (From Eberhardt and Huber, 2010)

Apparently, this isn’t just conjecture: male spiders have a lot of what the scientific community refers to as “slips” and “flubs” while trying to inseminate females. This whole business gets even more ridiculous when you look at the mazes some of those spiders have to traverse with their emboli.

Let me bring this image back.

Female spiders also have a curious lack of sensory organs, at least on the external portions of their genitalia (i.e., the area immediately surrounding their epigyne, technically called a spider vulva). Researchers are less sure about how sensitive the interior of the copulatory ducts and the spermatheca is- think of the size of the last spider you saw and try to imagine how tiny all these organs must be. It’s amazing they’ve figured out as much as they have.

Still, the female has got to have some sensitivity somewhere- a lot of spider behavior hinges on it. Lots of males prepare their palps by coating them with saliva to soften them, and then scraping areas on the female’s underside, perhaps to further signal his intent, or to stimulate her. Most continue to actively stridulate and stroke during sex, with one palp inserted and the other tapping rhythmically. The passion of some of these spiders often literally shakes the web.

(Please start playing this song in the background while watching this next video.)

But oh, we’re not done. The rather humble sounding short-bodied cellar spiders are among some of the most intense lovers of all, and the females tell them about it. Most spiders make little audible noise at all- it’s all sent via vibrations. But the female cellar spider actually squeaks by rubbing ridges on her chelicerae (fangs) and palps together. Researchers describe it as a sound similar to leather creaking, whatever that means.

This squeak is a negative one- it’s used in two contexts: when the female is chasing the male away because she doesn’t want to mate, and when she’s not happy with how things are going during sex. You see, the male short-bodied cellar spider has specialized, muscular palps. During copulation, he presses these palps up against his chelicerae so that the female’s epigyne is pinched, and then rotates his palps rhythmically for up to 40 minutes.

Spiderman digs it.

Apparently all this canoodling and doodling is a very good thing: more pinching and twisting seems to lead to larger clutch sizes when the female lays eggs. However, if he squeezes too hard, the female lets him know with a series of angry little squeaks until he desists. This, too, leads to higher fecundity; it pays to listen to her.

Bring back the sensual music as you read these excerpts from a scientific paper describing the sex between cellar spiders:

Very early in copulation each inward twist lasted for only about 2 s… Later the inward twists became longer and lasted for many seconds before the next outward twist… Still later the single outward twists were replaced by short bursts of twisting… Abdomen vibration was much more rapid during copulation… The strongest vibrations caused the male’s entire body to vibrate… (From Huber & Eberhard, 1997)

Whew, it’s getting a little warm in here, might want to open a window or something. These spiders might very well be too sexy for science.

Spider porn aside, most authors seem to agree that all these movements seem to be for one thing and one thing only: to stimulate the female. There aren’t many definitive answers as to how or why, but there’s a good chance that the female has stretch receptors inside her copulatory ducts and spermatheca so that she can feel when things are being pressed a certain way. The scientists claim that this is some measure of how the females can discern male fitness, but I’m fairly sure that the male spiders just like to treat a lady to a good time. You know, to thank her for not eating them.

No worries; not a stupid question at all. The dictionary definition of “genital” is “a person or animal’s external organs of reproduction,” so yes, by that definition male spider pedipalps- or rather, the palpal bulbs at the end- are considered genitals. (I personally think that definition’s broad enough to encompass a whole range of things, if you argue it right.)